huntia - Hunt Institute for Botanical Documentation

HUNTIA
A Journal of Botanical History
Volume 15 Number 1
2014
Hunt Institute for Botanical Documentation
Carnegie Mellon University
Pittsburgh
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Contents
De Bary’s legacy: The emergence of differing perspectives
on lichen symbiosis
M. E. Mitchell
Dr.Villars and his botanical disciples
Roger L. Williams
“Untersuchungen des Vorgangs bei der Befruchtung der Oenothereen”;
a translation of Wilhelm Hofmeister’s (1824–1877) 1847 paper on
fertilization in the Onagraceae (evening primrose family)
Michael Witty
Book Reviews and Announcements
5–22
23–45
47–58
59–70
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15(1) 2014
De Bary’s legacy: The emergence of differing perspectives
on lichen symbiosis
M. E. Mitchell
Abstract
Evidence that lichens exhibit algal and fungal
characteristics had been reported intermittently from
the 1760s onwards, but the signif icance of those
observations was not grasped until a century later. This
lapse is directly attributable to a blind endorsement by
contemporary botanists of the prevailing belief that
lichens constituted an autonomous category of plants.
The composite nature of lichens was first posited in 1866
and 12 years later the term “Symbiose” was proposed for
any union of dissimilar organisms; allegations that this
term was an unacknowledged borrowing from an 1876
publication are shown to be groundless. The present
paper surveys the — occasionally bizarre — attempts
over the last 100 years to delimit categories of lichen
symbiosis. Interpretations of biont interaction fluctuated
primarily between mutualism and parasitism until the
publication, early in the present century, of compelling
evidence that non-photosynthetic bacteria are involved
in the lichen symbiosis; this finding has made elucidation
of the alliance a still more distant prospect.
The work of documenting the various postulated
categories of symbosis had the unexpected result of
turning up primary references for sundry other lichenrelated terms. Since those references are widely dispersed
across the literature, an attempt has been made to
smooth the path of those wishing to source the names
of specific features by preparing a documented inventory
of all terms introduced in an exclusively lichen context
and currently employed; the results of that attempt,
chronologically and concisely presented, appear as an
addendum to this paper.
Introduction
The affinity between gelatinous lichens
and the genus Nostoc was first remarked on
late in the 18th century by Haller (1768, 3:94)
and Ventenat (1799, 2:36), at which time the
Department of Botany, National University of
Ireland, Galway, Ireland
5
conformity between fungal and lichen fruitbodies was also recognized by Hedwig (1787–
1797, 2:3) and Persoon (1794a, p. 7). Those
reports were underpinned in the opening
decades of the following century by Cassini
(1817, p. 396) in respect of Nostoc, by Fries
(1831, p. lxiii) with regard to the structure
of lichen sporocarps, and by Unger (1833,
p. 540) who observed “Protococcus” unicells
in thalli of Xanthoria (as Parmelia) parietina.
Such findings did not, however, lead to any
early understanding of lichen structure: by the
1840s virtually all botanists — hostages to “the
paralysing influence of the preconceived idea”
(Sprague 1933, p. 31) — endorsed the dictum of
Acharius (1810, p. 14) that lichens represented
an autonomous grouping distinct from either
algae or fungi.
Despite the emergence of further evidence to
the contrary, the Acharian view prevailed until
Anton de Bary (1831–1888) — while professor
of botany at the University of Freiburg — aired
the possibility that some algae “assume the form
of Collema, Ephebe etc. as a result of penetration
by certain parasitic ascomycetes” (1866,
p. 291).1 Simon Schwendener (1829–1919), then
at the University of Munich, was quick to grasp
the significance of de Bary’s intuition, which he
realized could apply to all lichens (Anonymous
1867). Further development of this insight
by Schwendener endorsed de Bary’s parasitic
assessment of the components’ relationship,
which the former vividly presented (1869, p. 3)
as that of a fungal taskmaster exploiting colonies
of algal slaves (“Sclaven”); Schwendener termed
6
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his interpretation “helotism” (“Helotenthum,”
p. 4). For most botanists, however, the notion
that a parasitic relationship could generate a
perennial organism was, at best, implausible,
and there were w idespread expressions
of dissent (cf. Sapp 1994, p. 6). Though
Schwendener (1872) addressed some of these,
it was not until the concept of symbiosis was
formulated later in the decade that a dual
constitution of lichens came gradually to be
accepted.
Perru (2006, p. 14) took the view that
though “[Albert] Frank [1839–1900] and
de Bary are the scientists whose names are
commonly mentioned in connection with
the origins of symbiosis … it appears more
and more unlikely that de Bary and Frank
coined the term symbiosis independently.”2
As his source for that contention, Perru cited
Richardson (1999) where the relevant passage
reads (pp. 641–642)
It is most unlikely that de Bary and Frank
independently invented the term symbiosis.
They worked at universities only 35 km
apart … and Frank not only used “symbiosis”
first but also introduced other terms such as
“mycorrhiza” (Frank, 1885). Hawksworth
(1995a) believes that de Bary either heard a
lecture by Frank on lichens, or a report of such
a lecture, and then adopted and introduced the
word “symbiosis” to his own audience a year
later. There seems to be no documentation to
show that they actually discussed “symbiosis”
but it is clear that de Bary admired Frank’s
research. He is mentioned both in the preface
of Comparative Morphology of Fungi, Mycetozoa
and Bacteria and again several times in the text
(de Bary, 1887). It is interesting, however,
that de Bary does not, as far as I can see, use
“symbiosis” anywhere in his book even though
it contains a substantial section on lichens.
This again suggests that he used the term in
his lecture after listening to Frank’s paper,
talking or corresponding with him and that
“symbiosis” was not a term that de Bary himself
coined and of which he was proud.
Taking that final, gratuitous, comment first, it
is incorrect to say that “de Bary does not … use
‘symbiosis’ anywhere in his book”: the word
is actually indexed in Comparative Morphology
with reference to page 356 where de Bary
wrote, “Fungi have long been divided into
two main sections founded on their nutritive
adaptation. Those which constitute the first
category feed on living organisms whether
plants or animals and are termed parasites.
Their relationship with their hosts is that of a
common life, a symbiosis. The others inhabit
decaying bodies and feed on dead organic
substances, and have been named therefore
since 1866 [Bary, p. 205] saprophytes.” As
regards the statement that “[t]here seems to
be no documentation to show that [de Bary
and Frank] actually discussed symbiosis,”
a belief that they did so appears to be the
reason for mentioning their having “worked
at universities only 35 km apart [Halle and
Leipzig].”3 If any such local discussions did
take place, they would necessarily have been
before early 1872, when de Bary became
professor of botany at Strasbourg (then
Strassburg, which it remained until 1919),
and would certainly not have found Frank
in a position to contribute usefully to any
discussion concerning lichen composition: as
late as September 1873, when addressing the
annual meeting of German Naturalists and
Physicians, held that year at Wiesbaden, Frank
(1873, p. 132) reported on an anatomical study
of Pertusaria pertusa (as Variolaria communis) that,
he claimed, demonstrated the production of
green cells by colorless thalline filaments or,
as he put it, “the development of gonidia from
hyphae.”4 It is possible that de Bary attended
Frank’s lecture and later explained to him
why he could not have made the observation
in question; if symbiosis were mentioned
during any such conversation, de Bary would
have been the only one in a position to do so.
In any event, three years later Frank (1876c)
had not alone come to regard lichens as
dual organisms but was proposing the term
“Symbiotismus” (p. 195) to describe the
component relationships.
Mitchell: De Bary’s legacy
In 1878, at Cassel, de Bary also addressed the
meeting of German Naturalists and Physicians.
He began by stating that he had chosen to
speak on “the phenomena associated with the
alliance of unrelated organisms — symbiosis,
as it may be put concisely and in general,” and
later commented (p. 124; p. 21 in the 1879
reprint) “parasitism, mutualism, lichenism
etc. are really at times special instances of
that general associative arrangement for
which the aforesaid term symbiosis may serve
as a collective designation. If one wishes to
differentiate between these main categories,
two may be emphasized: one antagonistic with
reciprocal conflict, and the other mutualistic,
in the wide sense, with complementar y
betterment of the symbionts.”5 Hertig et al.
(1937, p. 327) astutely remarked that “[t]he
almost casual way in which the term was
introduced” by de Bary “might give one the
impression that it had been used previously
in the biological literature” but “found no
reference to it earlier than the symbiosis
address”; they were, however, quite correct.
When the Greek botanist Theophrastus
(ca.370–ca.285 bc) described a particular
instance of ivy growing on the olive in
Historia Plantarum (2.1.2, Amigues translation,
2003, p. [44]), he applied the existing word
“sumbiosai” (“συμβιωσάί”) to the living
together of those plants; the word also appears,
in modified form though similar sense, in De
Causis Plantarum (2.17.5, Einarson and Link
translation, 1976, p. 338). Since we know that
de Bary had read Theophrastus (Bary 1853,
p. 103), it is reasonable to assume that memory
served him well when circumstances required.
There remains the fact that de Bary made
no mention of Frank’s paper either in his
lecture or the extensively annotated version
published in the following year (1879), yet he
could scarcely have been unaware of it because,
in the summer of 1876, the then widely
circulating journals Flora and Hedwigia carried
a “Preliminary Communication” (“Vorläufige
7 Mittheilung”) of its content (Frank 1876a,
1876b). But if having seen one or other of
these — both worded alike — de Bary deferred
a reading of Frank’s full 77-page report when
it appeared late in 1876, he would not have
met with Frank’s “Symbiotismus” because
the word does not appear in the “Preliminary
Communication.” The facts outlined above,
together with the range of terms credited to de
Bary by Wagenitz (2008), amply demonstrate
that an attempt to portray him as reduced to
cribbing is not rationally sustainable.6
The word spreads and the concept
broadens
At St r a sbou r g, de Ba r y c re ated a n
outstanding research institute where many
European and North American postgraduates
enjoyed the privilege of working under his
direction. Some of these men (all 68 of de
Bary’s Strasbourg postgrads were indeed male)
later made the idea of symbiosis familiar to a
wide public: among them, the German Georg
Klebs (1857–1920) produced an exhaustive
survey of the subject with reference to both
plants and animals (1882), the Italian Oreste
Mattirolo (1856–1947) produced a semipopular account (1883) restricted to plants
(then including fungi) and the Englishman
Frederick Bower (1855–1948) paused in his
study of vascular cryptogams to endorse
the — then still contested — judgement “that
lichens are not in themselves distinct plants,
but are a compound of fungi and algae, living
together in a relationship of mutual help called
‘symbiosis,’ (erroneously termed parasitism)”
(1887, p. 38).
Among de Bary’s peers, Eduard Strasburger
(1844–1912), professor of botany at the
University of Bonn, also helped popularize
the concept. He believed that lichens depend
for their existence on a mutualistic relationship
and, in one of the earliest comments on
lichen metabolism, personified them as “the
8
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15(1) 2014
proletarians among plants” (1891, p. 199) because
of the meager nutrient turnover available to
them for survival and reproduction.7 At this
time, symbiosis already accommodated — in
addition to mutualism — a ménage comprising
com mensa l ism, 8 consor t ism, 9 helot ism,
lichenism10 and parasitism, but some believed
still further categorization was needed. While
attached to the Forestry Research Institute at
the University of Munich, Karl von Tubeuf
(1862–1941) published a plant pathology
text (1895) that included a brief excursus
on the lichen association; taking the view
that mutualism did not adequately convey
such “unification of two living beings into
an individual whole,” he proposed that the
alliance be designated “Individualismus.”11
Later in the decade Wilhelm Zopf (1846–
1909), professor of botany at Münster and best
remembered by lichenologists for his work
on thallus chemistry, reported on a study
involving several fungi that he regarded as
lichen parasites. Zopf found that in some
instances the hyphae of those fungi do not
invade the host algae, a condition he termed
“Parasymbiose” (1897).12 Other instances of
Zopf ’s tripartite associations were published by
Alexandr Elenkin (1875–1942) while attached
to the St. Petersburg Botanical Garden. His
paper (1901) included the assertion that a
mutualistic interpretation of component
relations was incompatible with reports of
dead algal cells within thalli, a view that
led him to propose the jettisoning — in a
lichen context — of “symbiosis” in favor of
“endosaprophytism.” Despite further advocacy
in the following year, Elenkin failed to win
support for that proposal, but his views did
occasion debate at a time of particular Russian
concern with the phenomenon of symbiosis
(Khakhina 1992, pp. 51–54, 58, 90).
In 1905 Constant in Meresch kowsk y
(1855–1921), then lecturer in botany at Kazan
University, published the now celebrated
article in which he portrayed chloroplasts
a s s y mbiot ica l ly ad apted c ya nophy te s
(cyanoprokaryotes), and two years later Andrei
Famintsin (1835–1919), professor of botany
at the University of St. Petersburg, reported
brief ly on attempts to isolate and culture
“a chlorophyllous structure from plants,
lichen algae in particular” (1907, p. 355).13
Mereschkowsky’s revolutionary theorizing
failed to attract any early attention outside
Russia. It went unmentioned, for example, in a
wide-ranging review (1910) of advances in the
study of symbiosis by Zopf ’s assistant Friedrich
Tobler (1879–1957). Mereschkowsky again
aired his hypothesis in a comprehensive study
that represented cell organelles as exogenous
bodies, a concept he styled “Symbiogenesis”
(1910, p. 279), but that paper too was ignored
by most Western biologists for well over half
a century.
A mong the few prepared to keep an
open mind on the subject was the American
l ichenolog ist Br uce Fi n k (1861–1927),
professor of botany at Miami University,
Ohio. During the years immediately following
his appointment in 1906, Fink completed a
study of Minnesota lichens on which he had
been engaged for the previous ten years. The
introduction to that work extends to a brief
commentary on the topic of symbiosis in
the course of which Fink (1910, p. 7) stated
“we seem to have in lichens the highest
expression, so far as is known, of mutualism.”
In November 1909, however, Fink had
written to “75 American botanists and an
equal number of foreign botanists asking for
their views regarding the classif ication of
lichens” (1911, p. 231); essentially he hoped
to quantify the factions representing “those
who believe that lichens should be regarded as
fungi” and “those who think that these plants
form a group entirely distinct from fungi”
(p. 232). Of the 150 botanists circularized,
115 replied (Famintzin among them), and
Mitchell: De Bary’s legacy
some of their opinions evidently convinced
Fink that symbiont relations should properly
be interpreted as parasitic. In a further paper
(1913), while accepting “that the chlorophyll
granules of higher plants resemble certain
algae and may be such” (p. 103), Fink now
considered that even if proved this would not
validate “the mutualism hypotheses, to one
of which some of us had adhered for many
years” (p. 117), and declared it was “time to
be done with those unproved and hopeless
hypotheses of mutualism, consortism and
individualism” (p. 141). Such swaying between
mutualistic and parasitic interpretations
of the symbiosis became a lasting feature
of the debate. A contemporary of Fink’s,
the Ger man Wilhelm Nienburg (1882–
1932) — subsequently author of the first work
devoted to lichen anatomy — published an
account of lichen symbiosis (1913) in which he
too, harking back to Schwendener, visualized
the fungus as surviving at the alga’s expense:
“the fungus can make subtle adjustments to
its algal associate’s metabolism with the result
that the former is ultimately sustained by the
latter’s assimilates. Such dependency calls to
mind a prudent master whose careful provision
for his slaves enables him the better to exploit
them” (p. 938).14
This return to a perception of lichen
symbiosis as parasitism took a curious turn
when Fernand and Valentine Moreau (1886–
1980, 1886–1974), then working as assistants
at the Sorbonne, published the results of
an extensive anatomical study involving
species of Peltigera and Solorina (1919). Their
investigation of the cephalodia produced
by, in particular, P. aphthosa, led them to
interpret those structures as galls resulting
from the stimulator y effect of airborne
cyanoprokaryotes on cortical hyphae. The
Moreaus then went further, to the extent of
proposing that the entire thalli they had studied
were a response of the component fungus to
9 a biomorphogenetic stimulus delivered by the
alga: “we have come to regard the Peltigera
thallus as the equivalent of an organ deformed
by a parasite … this concept should probably
be broadened and extended to all lichens”
(p. 125).15 Their contemporaries were not
particularly taken by such assertions, Nienburg
(1926, p. 100) for example rejected them
as “absurd,” with Darbishire (1927, p. 222)
similarly, if less bluntly, dismissive; despite
Fernand Moreau’s periodic championing of
the gall concept in subsequent years, it never
attracted serious support.
A nother unor thodox ta ke on l ichen
symbiosis was published early in the 1920s by
Arthur Church (1865–1937), demonstrator in
botany at Oxford University. His belief that
fungi were “saprophytic and transmigrant
derivatives of marine algae of higher grade”
(1919, p. 63) led him to regard the lichen
alliance as a “case of an algal race, deteriorating
along the lines of a heterotrophic existence, yet
arrested, as it were, on the somatic downgrade,
by the adoption of intrusive algal units of
lower degree to subserve photosynthesis”
(1920, p. 267). If Church expected his brainchild to meet with general acclaim he was
to be majorly disabused: principal among
the very few contemporary lichenologists
to comment on the theory were Darbishire
(1924, p. 23; 1926, p. 753) and Smith (1921,
pp. 421–422), neither of whom was unduly
enthused. Though beyond question a very able
botanist — his illustrations of floral anatomy are
still widely admired — Church’s engagement
with symbiosis was not his finest hour.
A somewhat similar reception awaited
the views of Ewald Bachmann (1850–1937),
a retired Ger man second-level biolog y
teacher and author of numerous papers on
lichenological topics. Observations made in
the course of an anatomical study involving
Anaptychia, Cladonia, Schaereria and Umbilicaria
material led Bachmann (1923) to report a
10
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15(1) 2014
marked increase in the number of algal cells
at sites of incipient ascomatal and pycnidial
formation, and their gradual disappearance
as those structures matured. He consequently
assumed that the algae had become a source
of “nitrogen-rich material” (“sticksstoffreichen
Baustuffe”) for the fungal component (p. 239),
an inference that pointed to a parasitic
relationship and at odds, therefore, with
Bachmann’s firm conviction that symbiosis
was essentially mutualistic. To overcome this
problem, and influenced perhaps by Nienburg’s
(1913) analogy mentioned earlier, he contrived
a decidedly anthropomorphic interpretation of
his findings: “rather than indicating parasitism,
the case of algal cells being completely
resorbed during fruit development represents
their ‘sacrificial murder’ (‘Opfertod’) for the
benefit of the lichen fungus” (p, 253). He
believed “the expression ‘supportive slavery’
might well be applied to lichen algae were it
not that the fungal component suppresses their
sexual reproduction. That stumbling block is
removed, however, if the algae are compared to
castrated farm animals, prized by their master
as a highly valuable possession and treated
accordingly” (p. 254).16 Bachmann’s arresting
vision was at best coolly received by his peers
and, apart from a mention by Wallert (1931,
pp. 348–349), effectively forgotten.17
None of those who had so far concerned
themselves with the interaction of lichen bionts
doubted that they were dealing solely with
algae and fungi. However, in the course of a
study undertaken at the University of Urbino,
Maria Cengia Sambo (1888–1939) noted that
thalli of Pannaria rubiginosa and certain Peltigera
species consistently harbor bacterial cells in the
gelatinous sheaths surrounding their Nostoc
photobiont. Having tentatively assigned those
cells to the genus Azotobacter, she went on to
suggest that they contribute to the lichens’
metabolism by fixing atmospheric nitrogen,
and introduced the term “polisimbiosi” for
this tripartite association (1923, p. 236).
Subsequently, after she had moved to the
Plant Biology Laboratory at Florence, Cengia
Sambo expressed herself satisf ied that the
Nostoc-associated bacter ium did indeed
represent a species of Azotobacter (1925, p. 194).
In the short term, however, the concept of
polysymbiosis attracted scant attention, to
the extent that Friedrich Tobler, now director
of the Dresden Botanical Garden, made no
mention of it in the otherwise detailed review
of symbiosis that constitutes the fourth section
of his Biologie der Flechten (1925, pp. 167–216).18
A report on the growth of a lichenicolous
fungus within cephalodiate Lobaria pulmonaria
thalli, prepared at the University of Strasbourg
by Roger-Guy Werner (1901–1977), included
a claim that the invasive hyphae exhibit
a divergent response to contact with the
chlorophyllous organisms present. Werner
regarded the response he observed in hyphae
associated with the host’s algal cells as coming
within the compass of parasymbiosis but chose
to particularize the hyphal variation allegedly
discernible in the vicinity of the secondary
photobiont as “pseudoparasymbiose” (1928,
p. 203). Such finespun discrimination appears
to have been largely illusory, however, and
Werner’s coinage found no place in Abbayes’
(1937) commentary on contemporary work
in the area of lichen symbiosis. His review of
that literature led him to conclude that the
relationship definitely points — in the case of
most thalli — to “the alga giving more than it
receives,”19 and, consequently, that the symbiosis
concerned is, in effect, a parasitic association.
The question of bacterial involvement in
thallus metabolism had hung fire for well
over a decade when Pavel Henckel (1903–
1985) communicated the results of a study
undertaken at Perm State University. Having
noted the presence of Azotobacter in material
belonging to 11 micro- and macrolichen
genera — a circumstance he referred to as
Mitchell: De Bary’s legacy
triple symbiosis — Henckel made “a special
study of the question concerning the reciprocal
relationships of the lichens’ three components”;
here he found that Azotobacter occurs in
association with the algal cells, which supply
the bacteria with nutrients that enhance
their nitrogen-fixing capacity, and believed
“in general, the fungus effects its nutrition
osmotically at the expense of algal glucides
and ammonia produced by Azotobacter” (1938,
pp. 18–19). 20 Henckel seems to have been
unaware of Cengia Sambo’s work — there is
no mention of his findings being at odds with
her contention that symbiotic bacteria are
restricted to thalli having a Nostoc photobiont;
coincidentally, Cengia Sambo briefly revisited
the topic of polysymbiosis in 1939, an occasion
on which she somehow felt constrained to
describe a loose arrangement of algae and
fungi, allegedly characteristic of certain lichen
species, as hemisymbiosis (“emisimbiosi”).
A valuable appraisal of the more important
literature on lichen biology published up
to 1940 was provided by Reinhold Schaede
(1887–ca.1965) while attached to the University
of Breslau (Wrockław). His survey comprises
ten sections ranging from algal components
to water relations. The brevity of that devoted
to symbiont interaction (1943, p. 97) reflects
how few facts had then been established in
this regard, with Schaede saying only that
all intermediate stages exist from sustained
parasitism (termed “Dyssymbiose”), involving
death of the invaded cells, to compatibility
(“Eusymbiose”). His review concluded with a
line from Tobler (1934, p. 4): “lichen biology
in general and physiology in particular are
still almost untilled ground and call out for
cultivation!” 21 Tobler’s prayer was heard
early in the the 1940s when Anton Quispel
(1917–2008), a graduate student at Delft
Technical College and, subsequently, at
the Universities of Groningen and Leiden,
undertook extensive experimental work on
11 the nutrition and relationship of bionts isolated
from several foliose species; his findings left
him feeling “certainly justified to consider
the association as mutualistic” (1943–1945,
p. 525). Further results were, however, to
prompt a reconsideration of that conclusion
and occasion his obser vation (1951, pp.
69–70) that “[t]oo many biologists had failed
to realize that two organisms don’t enter into
a symbiosis to give something to a partner,
but in order to take as much advantage of the
partner as possible.” This view was endorsed
by Mackenzie Lamb (1911–1990), who, during
his tenure as director of the Farlow Herbarium,
judged the partnership to be one of “controlled
parasitism” (1959, p. 156), and by Mason Hale
(1928–1990) at the Smithsonian Institution,
employing the variant “balanced parasitism,”
(1961, p. 50). These further attempts to label a
condition for which there existed no empirical
data may have been the spark for Haynes’
(1964, p. 79) quip that “[s]ince the initial
discovery of the dual nature of the lichen
thallus, the only relationship that has not been
suggested between its components is one in
which neither partner affects the other.”
Interest in the physiology of lichen symbiosis
received an important stimulus when Vernon
Ahmadjian (1930–2012), professor of botany at
Clark University, published the first book to
deal solely with that subject (1967). The nature
of the relationship between the bionts was not,
however, discussed at length, with the author
content to say only (p. 78) that the alliance
could be expected to furnish instances of both
mutualism and parasitism. Neither of these
interpretations lacked for supporters, with those
backing the former perhaps more numerous
and imaginative: following a concise account
of lichen ecology and physiology, the German
plant physiologist Otto Stocker (1888–1979)
stated that “in the final analysis, organization of
the lichen symbiosis depends on the capacity of
the heterotrophic fungus to direct its hyphae to
12
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the construction of a ‘house’ for the storage of
rainwater and the supply of resources promoting
photosynthesis to the autotrophic tenant;
some of the latter’s metabolites go to pay the
landlord’s rent and so ensure survival of the
fungus. That two such differently constituted
partners should reach so successful a power
balance represents a natural ‘contrat social’ to
make politicians and sociologists die of envy.”22
This Rousseauvian parallel did not go untagged
as Stocker, using the German word for “rent,”
proceeded to encumber the literature with the
further notional category of “Mietsymbiose”
(1975, p. 370).
The majority perception of lichen symbiosis
as an essentially mutualistic union suffered
a reverse early in the 1980s. Having noted
the lack of any experimental evidence in its
support, Ahmadjian and Jacobs (1981, p. 169)
concluded from in vitro syntheses involving the
mycobiont of Cladonia cristatella and various
algae that “the relationship in this lichen is one
of controlled parasitism.” They subsequently
proposed that the fungal component of a lichen
be understood as a biotrophic parasite and the
symbiosis as a balanced alliance, in the sense
that “the percentage of cells killed is balanced
by new cells added to the population by
division of existing algal cells” (1983, p. 147).
Parasitism and several other postulates
concerning lichen biont interactions were
reviewed by Hale (1983, pp. 67–69) who
concluded that “[a]ll proposed concepts of
the relation between the fungus and alga in
lichens contain some elements of truth, but no
one theory can, in fact, embrace the complex
physiological activities that make lichen
symbiosis such a highly successful venture.”23
These wise words had, however, little impact in
the short term: for example, Hawksworth (1988,
p. 8) remained convinced that “the symbiosis has
to be viewed as mutualistic,” while Ahmadjian
(1993, p. 3) — speaking now of “balanced”
rather than “controlled” parasitism — described
mutualism as a “myth.”24 In fact, the lichen
symbiosis has to be regarded as just one among
the many associations visualized by Saffo (1993,
p. 23) as “too complex to pigeonhole into the
simple categories of parasitism, mutualism and
commensalism.”
While there had been sporadic comment
during the latter half of the 20th century
respecting the claim that bacteria contribute
to the lichen symbiosis, most of this was
uncompromisingly dismissive, e.g., Millbank
and Kershaw (1974, p. 298). Some years
into the new millenium, however, well
substantiated results demonstrating that nonphotosynthetic bacteria would have to be
factored into the lichen equation began to
appear (Cardinale et al. 2006, Hodkinson et al.
2006 and Bates et al. 2011). This development
has exposed the mutualism versus parasitism
debate as simplistic and further deferred an
understanding of the metabolic commerce that
sustains lichen growth.
Addendum: The naming of parts
Preparation of the above report on symbiotic
categories had the incidental result of bringing
to light the first appearance of various other
lichenological terms. As the corresponding
literature sources are nothing if not diverse,
it is hoped that the following attempt to
provide a brief but comprehensive itemizing
of the current lichen vocabulary will be of
benefit. General mycological terms pressed
into service by lichenologists over the years
are not considered here; only such designations
as were introduced with specific reference
to lichenized fungi are documented in the
following account.
The first feature of a lichen to be individually
characterized was the concave structure
produced by certain Cladonia species for
the deployment of their fruit-bodies. That
structure was termed an “acetabulum” by the
Swiss physician Jean Bauhin (1541–1612) in
Historia Plantarum Universalis (posthumously
Mitchell: De Bary’s legacy
published 1650–1651, 3:767). His lead in this
regard was followed by Tournefort (1700,
1:549) and Micheli (1729, p. 82), but the
German botanist Johann Dillenius (1687–1747)
preferred the word scyphus (1742, p. 75)25;
endorsement of this alternative by Linnaeus
(1753, 2:1151) ensured that it prevailed. No
further labelling occurred until the 1790s.
When Adanson (1763–1764, 2:11) established
the genus Graphis, he described the fruitbodies as furrows (“sillons”), a view endorsed
by the South African mycologist Christiaan
Persoon (1761–1836) in his statement that
“this very variable structure may be named
a lirella” (1794a, p. 3).26 Since just two lichenrelated terms were current at the end of the
18th century, contemporary mention of other
thalline features showed little consistency — a
shortcoming that would soon be addressed.
The emergence of lichenology as a distinct
discipline is largely attributable to the industry
of Erik Acharius (1757–1819), a native of
Gävle, eastern Sweden. Of Acharius’ many
publications, those that appeared in 1803,
1810 and 1814 amply justify his portrayal
as “the founder of the systematic study of
lichenology” (Arvidson 1999, p. 25). Acharius’
first contributions to terminology came in
Lichenographia Suecicae (1799), where, together
with nine now obsolete designations, he
described the pits occurring on the lower
cortex of Sticta species as cyphellae (p. xvi).
This was followed by a suite of terms that
have been familiar to lichenologists ever
since: apothecium, 27 cephalodium, 28 podetium,
proper margin, soredium, thallus (1803, pp. ix,
xix, xxii, xvi, xxi, vii, respectively); Acharius
subsequently added thalline margin (1810, p. 6)
and mazaedium (1817, p. 224). A selection of his
introductions was glossed for British botanists
by Gray (1821, 1:223–224), and in the case
of proper and thalline margin, the Swedish
mycologist Elias Fries (1794–1878) changed
the noun to exciple (1825, pp. 230) — all four
of which renderings remain current.
13 Primarily, of course, Acharius was the
author of many new genera, and one of these,
Isidium, was designed to accommodate species
characterized by the production of distinctive,
cortical, outgrowths. That genus was later
recognized as representing a quite artificial
assemblage, at which stage its name was applied
to a single such outgrowth by Georg Meyer
(1782–1856). Before his appointment to a
professorship at the University of Göttingen,
Meyer was “Economic Counsellor of the
British Crown in Hanover,” as rather grandly
stated on the title page of his Entwicklung,
Metamorphose und Fortpflanzung der Flechten
(1825). 29 The appearance in that work of
such expressions as “development of isidia”
(“Isidienbildung,” pp. 201, 207), “tops of
isidia” (“Isidienköpfe,” p. 204) and “shape
of isidia” (“Isidienform,” p. 206) made the
new usage familiar to a specialist readership
that soon gave it currency (e.g., Fries 1831,
p. lxxiv). Meyer was furthermore responsible
for prothallus, introduced in a discussion of
lichen growth (pp. 315–316).
A lso in 1825, the Ger man physician
Friedrich Wallroth (1792–1857) published
the first volume of Naturgeschichte der Flechten
(1825–1827). An able though self-opinionated
botanist, Wallroth was particularly critical of
Acharius, to the extent that he prepared an
alternative, largely Greek-based, terminology.
This would have presented little difficulty
to so accomplished a classicist, 30 but given
Wallroth’s addiction to periphrasis, the results
were so long-winded that he was publicly
censured (e.g., Martius 1826, pp. 209–210; Fée
1826, p. 362). Wallroth is now remembered
only for the designations epi- and hypophloeodal
(1825–1827, 1:141–142), the thalline categories
hetero- and homoiomerous (1:23–24) and the
word “gonidium” (1:40), which last continued
in everyday use until supplanted in the 1960s
(see Scott 1957 below).
Wallroth’s critic Carl von Martius (1794–
1868), professor of botany at the University of
14
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15(1) 2014
Munich, had spent the years 1817 to 1820 on
fieldwork in Brazil and reported on some of
the lichens collected there in the first part of
Icones Plantarum Cryptogamicarum (1828–1834).
Here, on the basis of painstaking microscopical
investigation involving Cladonia, Collema,
Lecidea and Parmelia material, he described
and illustrated the hypothecium (pp. 23–30,
pls. 23–24). Hypothallus also dates from this
time and is attributable to Fries (1831, p. xxix)
who, though happy as we have seen to endorse
Meyer’s use of isidium, sought to replace his
prothallus with this new term. In the event,
both designations came to be used and have
proved a recurrent source of confusion (see
Hannemann 1973 below). By the early 1830s
the number of thalline features whose names
remain in current use had reached 21, and there
the figure remained for the following 20 years.
Towa rd s m id- cent ur y, good qua l it y
microscopes were in the hands of a privileged
few, among them Julius von Flotow (1788–
1856), a Prussian army officer, who expressively
described how the acquisition of a Schiek
instrument had furthered his researches (1850,
p. 361). Flotow paid special attention to crustose
lichens, work on one of which — Rimularia (as
Mosigia) gibbosa — led to his recognizing the
epithecium (1851, p. 776). In the area of lichen
anatomy the most accomplished microscopist
of the period was, however, Louis-René
Tulasne (1815–1885). Beginning in 1842,
Tulasne spent 30 years as an assistant at the
Natural History Museum in Paris where his
work earned him renown as a mycologist.
Initially he took a particular interest in lichens,
and in 1852 published an innovative anatomical
and morphological study of the group, which
included his description and naming of the
pycnidium (p. 108). For much of the period
from 1850 to the early 1870s, Tulasne had
the expatriate Finn William Nylander (1822–
1899) as an unofficial colleague at the Museum.
Nylander’s unremitting nomenclatural drive
was not ref lected, fortunately perhaps, in
his engagement with terminology: here his
contributions numbered just four, the earliest
of which were hymenial algae (as “gonidia”)
and the use of thecium as an alternative to
“hymenium” (1853, p. 158, fn.).
The first relevant contribution from a British
lichenologist appeared about this time. In a
prefatory comment to his survey of the genus
Arthonia, the clergyman William Leighton
(1805–1889) drew attention to the fact that
when Acharius introduced that generic name,
he wished to convey his perception of the fruitbodies as sprinkled over the thallus but, in the
process, had somehow used “artho” instead of
“ardo.” Consequently, when Leighton decided
there was need, he chose “to designate the
[Arthonia] apothecium by the term ardella,
significant of its appearance as a sprinkled spot”
(1854, p. 437).31 With microscopes becoming
more readily available, spore morphology
began to receive close attention as a source
of generic criteria. One advocate of this
approach was Wilhelm Koerber (1817–1885),
professor of botany at the University of Breslau
(Wrockław); he described the distinctive
spores of Rhizocarpon and Umbilicaria, for
example, as muriform (1855, p. 443) and those
of Xanthoria as “polari-dyblastae” (p. 91;
anglicized to “polari-bilocular” by Mudd
(1861, p. 11) and abbreviated by the French
abbé Henri Olivier (1849–1923) to polarilocular
(1882–1884, 1:14)). Koerber also coined
amphithecium (1855, p. 321), which, being of
obscure application, was soon lost to view and
so remained until reintroduced some 40 years
later (see Darbishire 1898 below). Activity in
the 1850s concluded with, first, Nylander’s
remaining contributions, viz. chondroid axis
and pseudocyphella (1858–1869, 1:266, 333),
and, secondly, the publication by Theodor
Fries (1832–1913) — son of Elias Fries and
also, eventually, professor at Uppsala — of
a commentary on the genus Stereocaulon in
Mitchell: De Bary’s legacy
which he added phyllocladium to the growing
tally, though clearly with reluctance (1858,
p. 315, fn.).
The three decades following the 1850s
proved a good deal less productive. Goniocyst
was introduced by Johannes Norman (1823–
1903), a Norwegian forester (1872, p. 10),32
campylidium by Johannes Müller (1828–1896),
professor of botany at the University of Geneva
(1881, p. 111), and pseudopodetium by Gustav
Krabbe (1855–1895) while a research student
at the University of Berlin (1882, p. 108).33 The
years to century’s end brought a return to form
with the emphasis on anatomical attributes.
First, however, Vainio (1890, p. xxiii) proposed
the use of pseudostroma in the case of lichenized
fungi. Then in an extensive study of cortical
structure and its bearing on water relations,
Hugo Zukal (1845–1900) — working at a
teacher training institute in Vienna — identified
the pallisade hyphae that characterize the
Roccella cortex (1895, p. 1306). As originally
conceived by Acharius in 1803, the soredium
denoted a specific cortical area, but later the
word also became applied to an individual
diaspore produced in such areas; this dual usage
continued until Johannes Reinke, professor of
botany at the University of Kiel, proposed that
the diaspore-producing areas be named soralia
(1895, p. 380, n. 1). At the same time, Otto
Darbishire (1870–1934) — Reinke’s Welsh
assistant — was engaged on a monograph of the
genus Roccella, work that led to his designating
the amphithecium and parathecium (1898, p. 7).34
The 1890s ended with a proposal by Gustav
Lindau (1866–1923), then at the University of
Berlin, that the vague term “pseudoparenchyma”
be replaced by plechtenchyma, to which the
prefixes para- and proso- could be appended as
required (1899, p. 7); this initiative quickly won
general support.
The opening decade of the new century
produced three additions: Arthur Minks (1846–
1908), in medical practice at Stettin, published
15 a revision of the genus Umbilicaria in which an
unreported propagule became a thyllale (1900,
p. 17), Elenkin (1902, pp. 75, 83) reported a
necral layer in certain crustose thalli, and the
French abbé Auguste-Marie Hue (1840–1917)
labelled the fastigiate cortex (1906, p. 243). There
then followed a period of almost 40 years during
which no currently employed additions were
made to the terminological inventory.
Postwar, a return to the logging of thalline
features was initiated by two Swedish workers.
Einar Du Rietz (1895–1967), professor of plant
ecology at the University of Uppsala, suggested
replacing epi- and hypothecium with epi- and
subhymenium (Nannfeldt and Du Rietz 1945,
p. 86); this did not happen, however, and all
four terms have so far stayed the course. Gunnar
Degelius (1903–1993), then also at Uppsala,
described a new asexual propagule observed
on Lempholemma cladodes material as a hormocyst,
produced within a hormocystangium (1945).
Monographic studies of, first, Umbilicaria by
George Llano (1910–2003), working at the
Smithsonian Institution, introduced gyro-, leioand omphalodisc (1950, p. 5), while Degelius
(1954, p. 56) distinguished between the euand pseudocortex in Collema. Also in that work
(p. 50, fn.), Degelius revived earlier objections
to the practice of describing the chlorophyllous
cells of lichens as “gonidia,” and three years
later George Scott (1927–), at the University
of Glasgow, proposed that lichen components
be known as mycobionts and phycobionts.35
Scott’s recommendations soon became
generally accepted, as for example by the
German specialist on fruit-body development,
Aino Henssen (1925–2011), in the work
that contributed pycnoascocarp (1963, p. 20).
Shortly afterwards, her compatriot Josef
Poelt (1924–1995), whose career began at the
Botanische Staatssammlung in Munich, gave
the first evidence of his terminological flair
with the coining of schizidium (1965, p. 581)
and epipsamma (1969, p. (32)). In the following
16
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15(1) 2014
decade, Poelt’s for mer student Br ig itte
Hannemann (ca.1940–) distinguished the
rhizinomorph of Umbilicaria and, in connection
with Anzia, proposed that spongiostratum replace
hypothallus, which “is used for very different
things” (1973, pp. 8–9). 36 The other 1970s
introductions were reported by the Czech
Antonín Vězda (1920–2008) for hyphophore
(1973, p. 82), the Norwegians Eilif Dahl
(1916–1993) and Hildur Krog (1922–2014)
for pseudoisidium (1973, p. 13),37 Henssen and
Jahns (1973, p. 99) for thallinocarp, Poelt (1974,
p. 107) for phyllidium, the British physician
Dougal Swinscow (1917–1992) and Hildur
Krog for dactyl (1978, p. 162), and Hasenhüttl
and Poelt (1978, p. 276) for thalloconidium. The
following decade was equally fruitful, with
the asexual diaspores blastidium and thlassidium
being named by Poelt (1980, p. 23; 1986, p. 16),
polysidium by Kalb (1987, p. 18) and parasoredium
by Poelt in collaboration with Codogno et al.
(1989, p. 67, fn.); new thalline features were
also distinguished at this time under the names
paracephalodium (Poelt and Mayrhofer 1988,
p. 279) and phenocortex (Poelt 1989, p. 67, fn.).
This survey ends with the year 2000, which
leaves just two coinages to be accounted for:
that by Tor Tønsberg (1948–), University of
Bergen, in respect of consoredium (1992, p. 34),
and photomorph introduced by Jack Laundon
(1934–), long associated with the Natural
History Museum, London, to impose order
on a ravelled synonymy (1995).
Acknowledgments
I wish to record my deep indebtedness to the
following colleagues: Professor R. Piervittori, University
of Turin, for generously providing a photocopy of
Oreste Mattirolo’s 1883 publication; the ILL team at
the Library, National University of Ireland, Galway,
for their unfailing help; and the members of staff who
obligingly supplied copies of material in their care at the
British Library, Cambridge University Library, Natural
History Museum, London and Royal Botanic Gardens
Library, Kew.
My frequent and helpful visits to the internet have
also to be gratefully recorded.
Notes
1. “ … sie nehmen die Form der Collemen, Epheben
u. s. f. an, dadurch, dass gewisse parasitische
Ascomyceten in sie eindringen.”
2. “Frank et de Bary sont les deux savants dont
le nom est généralement invoqué lorsqu’il
est question des origines de la symbiose … il
paraît de plus en plus improbable que de Bary
et Frank aient inventé le terme de symbiose
indépendamment l’un de l’autre.”
3. De Bary had moved to Halle in 1867.
4. “ … die Gonidien von den Hyphen abstammen.”
5. “ … eine Betrachtung der Erscheinungen
des Zusammenlebens ungleichnamiger
Organismen, der Symbiose, wie man kurz
und und allgemein sagen kann, zu wählen”;
“Parasitismus, Mutualismus, Lichenismus u.
s. w. sind eben jeweils bestimmte Specialf älle
jener allgemeinen Associationseinrichtung, für
welche der vorangestellte Ausdruck Symbiose
als Collectivbezeichnung dienen mag. Will man
unter dieser Hauptkategorien unterscheiden,
so dürften sich deren zwei herausstellen, die
antagonistische mit gegenseitiger Bekämpfung
und die in weiterem Sinne mutualistische mit
gegenseitiger Förderung der Symbionten.”
6.In the interests of historical accuracy, the opening
sentence of the entry for symbiosis in Kirk et al.
Dictionary of the Fungi (2008) needs to be revised.
7. “Sie sind die Proletarier unter den Pflanzen,
müssen sich mit schlechter Nahrung begnügen
und oft am Hungertuche nagen.”
8.The concepts of commensalism and mutualism were
introduced by Van Beneden (1873, pp. 785, 790).
9.The term “consortium,” mentioned in passing
by de Bary in his 1878 lecture, has been widely
attributed to Johannes Reinke (1849–1931),
lecturer in botany at the University of Göttingen
and subsequently professor at Kiel. In a report
on the occurrence of Nostoc cells in stems of
Gunnera tinctoria, Reinke (1872, p. 108) described
the association as a consortium, stating that
the word had been suggested by his colleague
August Grisebach (1814–1879); he subsequently
recorded (1894, pp. 525–526) that the suggestion
was made in the summer of 1872. As luck would
have it, that venerable Latin word had already
been chosen by Ferdinand Cohn (1828–1898),
professor of botany at the University of Breslau
(Wrockław), in January 1872 to describe the
lichen association (1873, p. 69). Reinke (1894,
p. 529) expressed keen resentment at de Bary’s
not having cited his paper when mentioning
“Flechtenconsortium” (1878, p. 126 ; 1879
reprint, p. 29), but de Bary’s silence in this regard
Mitchell: De Bary’s legacy
may reasonably be attributed to his having been
aware that the word’s use in a biological sense did
not originate with Reinke.
10.The first appearance of this term has not been
located.
11.The English translation is from Tubeuf (1897, pp.
86–87).
12.This relationship was interpreted as
“commensalistic” by Rambold and Triebel (1992,
p. 18) on the grounds that both fungi “share one
and the same nutritive source, the photobiont of
the host.”
13. “ … habe ich fortwährend, an die Flechtenfrage
anknüpfend, mich bemüht, aus Pflanzen, den
Gonidien entsprechend, einen chlorophyllhaltigen
Organismus auszuscheiden und ihm zum
selbständigen Leben zu zwingen.”
14. “ … weiß der Pilz die Entwickelung der
Algen ganz genau seinem eigenen Wachstum
anzupassen, so dass schließlich alle ihre Assimilate
ihm wieder zugute kommen. Er gleicht einem
klugen Herren, der seine Sklaven gut füttert,
damit er sie dann um so besser ausnutzen kann.”
This interpretation was further promoted by
Nienburg (1917, pp. 543–544).
15. “ … nous avons considéré le thalle aérien d’une
Peltigéracée comme l’équivalent d’un organe
déformé par un parasite … [c]ette notion doit
sans doute être élargie et étendue aux Lichens en
général.”
16. “Der Fall, daß bei der Fruchtentwickelung
Gonidien gänzlich resorbiert werden, ist kein
Anzeichen von Parasitismus, sondern ein
‘Opfertod’ zum Besten des Flechtenpilzes.”
“Deshalb würde auf sie der Ausdruck
‘wohlwollende Sklaverei’ viel besser anwendbar
sein, wenn die Gonidien durch den Flechtenpilz
nicht an der geschtlechtlichen Vermehrung
gehindert würden. Aber auch diese Klippe
wird umschifft, wenn man die Gonidien mit
kastrierten Haustieren vergleicht, die von
ihrem Herrn, dem Flechtenpilz, als wertvollstes
Besitzum geschätzt und dementsprechend
behandelt werden.”
17. Eventually, however, its second element would
be formulated anew to become “the common
model of the lichen symbiosis as a ‘domestication’
of photosynthetic algae by heterotrophic fungi”
(Piercey-Normore and DePriest 2001, p. 1496).
18.Any incidental standing that Cengia Sambo’s
work did enjoy would have suffered by association
when the Rhodobacterium cells reported from
Herpothallon (as Chiodecton) sanguineum by Uphof
(1925) proved to be crystals of chiodectonic acid
(Kolumbe 1927).
19. “ … l’Algue donnant plus qu’elle ne reçoit.”
17 20. “L’auteur … examine spécialement la question
concernant les rapports réciproques entre les trois
components du lichen”; “en général la nutrition
du champignon s’effectue osmotiquement aux
dépens des glucides de l’algue et de l’ammoniaque
de l’Azotobacter.” Other Russian work of
the period on lichen bacteria is discussed
by Khakhina (1992, pp. 92–93) where the
transliteration “Genkel`” is used as an alternative
to “Henckel.”
21. “Flechtenbiologie im allgemeinen, Physiologie im
besonderen sind noch fast unbeackerte Gebiete
und rufen nach Bestellung!”
22. “Letzten Endes beruht also die Organisation
der Flechtensymbiose darauf, daß der
heterotrophe Pilz konstitutionell bef ähigt
ist, seine Hyphenstruktur zu einem den
atmosphärischen Niederschlag sammelnden
“Haus” auszubauen, in welchem der autotrophe
Mieter die Arbeitsbedingungen für eine
photosynthetische Produktion findet und aus
ihr dem Hausbesitzer eine Miete bezahlt, die
dem Pilz seinen Lebensunterhalt sichert. Zwei
Partner so verschiedener Konstitution zu einem
so erfolgreichen Gleichgewicht der Kräfte
zusammenzubringen, is ein “contrat social” der
Natur, vor dem Soziologen und Politiker vor
Neid nur erblassen können.”
23.The case for regarding symbiosis as solely a
collective term was cogently put at this time by
Lewis (1985).
24.Ahmadjian’s pronouncement was not widely
influential: 17 years later Chapman and Chapman
(2010) still had reason “to attack the very
common misconception that lichens are a classic
example of mutualistic symbiosis between an alga
and a fungus” (p. 549) and to declare “the simple
and incorrect notion that lichens are examples of a
mutualistic (‘stress-free’) symbiosis really must be
put to rest!” (p. 554).
25.All current lichenological terms are italicized on
first citation here.
26. “Dieser sehr abweichenden Bildung könnte man
den Namen Lirella geben.”
27. Some confusion surrounds this term and
“perithecium.” The latter has been attributed to
Acharius (e.g., Ainsworth 1976, p. 96) but was, in
fact, coined by Persoon (1794b, p. 64) who used
it to indicate a tissue enclosing the “actual seed
capsules” (“die eigentlichen Saamenkapseln”)
in certain non-lichenized fungi. Those
capsules — today’s asci — were then also known
as thecae, which Persoon described as sometimes
forming a continuous layer or “hymenium” (p. 65);
he did not use thecium as an individual term and
neither, it seems, did any one else until Nylander
18
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15(1) 2014
more than 50 years later. Acharius’ apothecium
has been stated to derive from “apo- away + Gr.
thēkē case or cup” (Snell and Dick 1957, p. 10), but
Acharius made quite clear that he was using, in its
sense of “repository,” an existing word common to
Greek and Latin. Perithecium was first applied to
lichen fruit-bodies by Fries (1831, pp. lxvii, 8).
28. Here Acharius restricted the term to several types
of fruit-body, and others followed suit for a good
many years, despite his later having also applied
it to the cortical productions characteristic of
Peltigera aphthosa (1810, p. 517).
29. “Königlich Grossbritannisch Hannoverschem
Oekonomie-Rathe.”
30. Wallroth practised in the town of Nordhausen,
where he had the phycologist Friedrich Kützing
(1807–1893) as a colleague. When the first volume
of Tabulae Phycologicae appeared in 1845, a friend
expressed astonishment at the elegant Latin of the
Introduction, to which Kützing replied, “Wallroth
hat’s geschrieben” (Osswald 1896, p. 25).
31.The mistake was first pointed out by Fée (1824,
p. xxxi).
32.The status of the terms goniocyst and
goniocystangium (Santesson 1968, p. 181) has been
reviewed by Sérusiaux (1985, pp. 2–13) and
Sérusiaux et al. (2006, pp. 118–119).
33. Krabbe believed that his new type of secondary
thallus was peculiar to just one member of the
Cladoniaceae — Pycnothelia (as Cladonia) papillaria.
The Finnish Cladonia monographer Edvard Vainio
(1853–1929) soon showed that the development of
P. papillaria podetia does not, in fact, exhibit the
features claimed by Krabbe, but at the same time
ensured the survival of “pseudopodetium” by
applying that designation to the secondary thallus
of Stereocaulon (1887, pp. 53–54).
34. Darbishire was very likely unaware of Koerber’s
priority in respect of amphithecium — an
understandable lapse given that only Tuckerman
(1872, p. 245) and Vainio (1890, p. xxiii, n. 2)
appear to have mentioned the word.
35. Schneider (1895, p. 497, fn.) had declared that
“[g]onidia and related terms as ‘gonimia,’
‘gonidimia,’ etc., are meaningless in modern
lichenology, and should therefore be rejected,” a
view echoed by Fink (1922, p. 116) and Thomas
(1939, p. 163). When what had been known
as blue-green algae came to be recognized as
prokaryotes, Ahmadjian (1982) recommended
that the “[p]hotosynthetic symbionts of lichens
should together be referred to as photobionts,”
while also introducing cyanobiont and recycling
phycobiont to designate lichens’ blue-green and
green cells, respectively.
36. “ … der für verschiedenste Dinge benutzt wird.”
37.Unaware of this report, Awasthi (1975, p. 13) and
Vězda (1979, p. 48) applied the term to different
structures. In the same decade, Hale (1973, p. 3)
used the term epicortex in the belief that this was a
fresh coinage, but it had already been introduced
in a mycological context by Lohwag (1941, p. 122).
References
Abbayes, H. des. 1937. Considérations sur la symbiose
lichénique et ses différentes modalités. Bull. Soc.
Sci. Bretagne 14: 130–136.
Acharius, E. 1799 (1798). Lichenographiae Suecicae
Prodromus. Linköping: Björn.
Acharius, E. 1803. Methodus qua omnes detectos
Lichenes. Stockholm: Ulrich.
Acharius, E. 1810. Lichenographia Universalis.
Göttingen: Danckwerts.
Acharius, E. 1814. Synopsis Methodica Lichenum.
Lund: Svanborg.
Acharius, E. 1817. Af handling om de cryptogamiske
vexter, som komma under namn af Calicioidea. 3.
Kongl. Vetensk. Acad. Handl. 1817: 220–244.
Adanson, M. 1763–[1764]. Familles des Plantes. 2 vols.
Paris: Vincent.
Ahmadjian, V. 1967. The Lichen Symbiosis. Waltham:
Blaisdell.
Ahmadjian, V. 1982. Holobionts have more parts.
Newslett. Int. Assoc. Lichenology 15: 19.
Ahmadjian, V. 1993. The Lichen Symbiosis, ed. 2.
New York: Wiley.
Ahmadjian, V. and J. B. Jacobs. 1981. Relationship
between fungus and alga in the lichen Cladonia
cristatella Tuck. Nature 289: 169–172.
Ahmadjian, V. and J. B. Jacobs. 1983. Algal-fungal
relationships in lichens: Recognition, synthesis
and development. In: L. J. Goff, ed. 1983. Algal
Symbiosis: A Continuum of Interaction Strategies.
Cambridge: Cambridge University Press. Pp.
147–172.
Ainsworth, G. C. 1976. Introduction to the History of
Mycology. Cambridge: Cambridge University Press.
Anonymous. 1867. Protokoll der botanischen Sektion.
Verh. Schweiz. Naturf. Ges. 51: 88–91.
Arvidsson, L. 1999. A survey of lichenology in
Sweden during the 19th century. Acta Univ.
Upsal., Symb. Bot. Upsal. 32(2): 23–60.
Awasthi, D. D. 1975. A Monograph of the Lichen
Genus Dirinaria. Vaduz: Cramer.
Bachmann, E. 1923. Über das Verhältnis der Gonidien
zum Flechtenpilz. Hedwigia 64: 233–255.
Bary, A. de. 1853. Untersuchungen über die
Brandpilze und die durch sie verursachten
Krankheiten der Pflanzen. Berlin: Müller.
Mitchell: De Bary’s legacy
Bary, A. de. 1866. Morphologie und Physiologie
der Pilze, Flechten und Myxomyceten. Leipzig:
Engelmann.
Bary, A. de. 1878. Ueber Symbiose. Tagebl. Versamml.
Deutsch. Naturf. Aerzte Cassel 1878: 121–126.
Bary, A. de. 1879. Die Erscheinung der Symbiose.
Strassburg: Trübner.
Bary, A. de. 1887. Comparative Morphology and
Biology of the Fungi, Mycetozoa and Bacteria,
transl. H. E. F. Garnsey and I. B. Balfour. Oxford:
Clarendon Press.
Bates, S. T., G. W. G. Cropsey, J. G. Caporaso, R.
Knight and N. Fierer. 2011. Bacterial communities
associated with the lichen symbiosis. Appl.
Environm. Microbiol. 77: 1309–1314.
Bauhin, J. 1650–1651. Historia Plantarum Universalis.
3 vols. Yverson: N.p.
Bower, F. 1887. Schwendener’s theory of the nature
of lichens. Trans. & Annual Rep. Manchester
Microscop. Soc. 1887: 37–46.
Cardinale, M., A. M. Puglia and M. Grube. 2006.
Molecular analysis of lichen-associated bacterial
communities. F. E. M. S. Microbiol. Ecol. 57:
484–495.
Cassini, H. 1817. Doutes sur l’origine et la nature du
Nostoc. J. Phys. Chim. Hist. Nat. Arts 84: 395–399.
Cengia Sambo, M. 1923. Polisimbiosi nei licheni a
cianoficee e significato biologico dei cefalodi. Atti
Soc. Ital. Sci. Nat. 62: 226–238.
Cengia Sambo, M. 1925. Ancora della polisimbiosi nei
licheni ad alghe cianoficee. I batteri simbionti. Atti
Soc. Ital. Sci. Nat. 64: 191–195.
Cengia Sambo, M. 1939. Commensalismo utile nei
licheni o emisimbiosi. Nuovo Giorn. Bot. Ital., n.s.
45: xliv–xlvii.
Chapman, R. L. and M. R. Chapman. 2010. Green
algae and fungi in lichens: Symbionts — but friends
or foes? In: J. Seckbach and M. Grube, eds. 2010.
Symbiosis and Stress: Joint Ventures in Biology.
Dordrecht: Springer. Pp. 549–555.
Church, A. H. 1919. Thalassiophyta and the Subaerial
Transmigration. Bot. Mem. 3: 1–95.
Church, A. H. 1920. The lichen symbiosis. J. Bot. 58:
262–267.
Codogno, M., J. Poelt and D. Puntillo. 1989.
Umbilicaria freyi spec. nova und der Formenkreis
von Umbilicaria hirsuta in Europa (Lichenes,
Umbilicaraceae). Pl. Syst. Evol. 165: 55–69.
Cohn, F. 1873. Bericht über die Thätigkeit der
botanischen Section der Schlesischen Gesellschaft
im Jahre 1872. Jahresber. Schles. Ges. Vaterl. Cult.
50: 69–173.
Dahl, E. and H. Krog. 1973. Macrolichens of
Denmark, Finland, Norway and Sweden. Oslo:
Universitetsforlaget.
19 Darbishire, O. V. 1898. Weiteres über die
Flechtentribus der Roccellei. Ber. Deutsch. Bot.
Ges. 16: 6–16.
Darbishire, O. V. 1924. Some aspects of lichenology.
Trans. Brit. Mycol. Soc. 10: 10–28.
Darbishire, O. V. 1926. The structure of Peltigera
with especial reference to P. praetextata. Ann. Bot.
(Oxford) 40: 727–758.
Darbishire, O. V. 1927. Über das Wachstum der
Cephalodien von Peltigera aphthosa L. Ber. Deutsch.
Bot. Ges. 45: 221–228.
Degelius, G. 1945. Lichenisierte Hormocysten, ein
neuer Diasporentypus der Flechten. Svensk Bot.
Tidskr. 39: 419–430.
Degelius, G. 1954. The lichen genus Collema in
Europe: Morphology, taxonomy, ecology. Symb.
Bot. Upsal. 13: 1–499.
Dillenius, J. J. 1742 (1741). Historia Muscorum.
Oxford: Sheldonian Theatre.
Elenkin, A. 1901. Les lichens facultatifs (title of
résumé, original title of article in Russian). Izv.
Imp. S.-Peterburgsk. Bot. Sada 1: 129–154.
Elenkin, A. 1902. Zur Frage der Theorie des
“Endosaprophytismus” bei Flechten (title of
résumé, original title of article in Russian). Izv.
Imp. S.-Peterburgsk. Bot. Sada 2: 65–84.
Famintzin, A. 1907. Die Symbiose als Mittel der
Synthese von Organismen. Biol. Centralbl. 27:
353–364.
Fée, A.-L.A. 1824. Essai sur les Cryptogames des
Écorces Exotiques Officinales. Paris: Didot.
F[ée], A.[-L.-A.] 1826. Lichens. In: J. V. Audouin
et al., eds. 1822–1831. Dictionnaire Classique
d’Histoire Naturelle. 17 vols. Paris: Rey and
Gravier. Vol. 9. Pp. 360–369.
Fink, B. 1910. The lichens of Minnesota. Contr. U.S.
Natl. Herb. 14: i–viii, 1–269, ix–xvii.
Fink, B. 1911. The nature and classification of
lichens — I. Views and arguments of botanists
concerning classification. Mycologia 3: 231–269.
Fink, B. 1913. The nature and classification of
lichens — II. The lichen and its algal host.
Mycologia 5: 97–166.
Fink, B. 1922. Lichens. Bot. Gaz. 74: 115–117.
Flotow, J. von. 1850. Mikroskopische Flechtenstudien.
Bot. Zeitung (Berlin) 8: 361–369.
Flotow, [ J.] von. 1851. Aus Briefen von v. Flotow
über Psora privigna (Ach.) Fw. 1848. Bot. Zeitung
(Berlin) 9: 753–776.
Frank, [A. B.] 1873. Ueber das Verhalten der Gonidien
im Thallus einiger homöomerer und heteromerer
Krustenflechten. Tagebl. Versamml. Deutsch.
Naturf. Aerzte Wiesbaden 1873: 132.
Frank, A. B. 1876a. Ueber die biologischen
Verhältnisse des Thallus einiger Krustenflechten.
Flora 59: 303–304.
20
Huntia
15(1) 2014
Frank, A. B. 1876b. Ueber die biologischen
Verhältnisse des Thallus einiger Krustenflechten.
Hedwigia 15: 98–100.
Frank, A. B. 1876c. Ueber die biolgischen Verhältnisse
des Thallus einiger Krustenflechten. Beitr. Biol.
Pflanzen 2: 123–200.
Fries, E. 1825. Systema Orbis Vegetabilis. Lund:
Typographia Academica.
Fries, E. 1831. Lichenographia Europaea Reformata.
Lund: Berling.
Fries, T. M. 1858. Monographia Stereocaulorum et
Pilophorum. Nova Acta Regiae Soc. Sci. Upsal.,
ser. 3. 2: 307–380.
Gray, S. F. 1821. A Natural Arrangement of British
Plants. 2 vols. London: Baldwin, Cradock and Joy.
Hale, M. E. 1961. Lichen Handbook. Washington,
D.C.: Smithsonian Institution.
Hale, M. E. 1973. Fine structure of the cortex in
the lichen family Parmeliaceae viewed with the
scanning-electron microscope. Smithsonian Contr.
Bot. 10: 1–92.
Hale, M. E. 1983. The Biology of Lichens, ed. 3.
London: Arnold.
Haller, A. von. 1768. Historia Stirpium indigenarum
Helvetiae inchoata. 3 vols. Bern: Societas
Typographica.
Hannemann, B. 1973. Anhangsorgane der Flechten.
Lehre: Cramer.
Hasenhüttl, G. and J. Poelt. 1978. Über die
Brutkörner bei der Flechtengattung Umbilicaria.
Ber. Deutsch. Bot. Ges. 91: 275–296.
Hawksworth, D. L. 1988. The variety of fungal-algal
symbioses, their evolutionary significance, and the
nature of lichens. Bot. J. Linn. Soc. 96: 3–20.
Haynes, F. N. 1964. Lichens. Viewpoints Biol. 3: 64–115.
Hedwig, J. 1787–1797. Descriptio et Adumbratio
microscopico-analytica Muscorum Frondosorum.
4 vols. Leipzig: Müller.
Henckel, P. A. 1938. Sur la symbiose chez les lichens
(title of résumé, original title of article in Russian).
Byull. Moskovsk. Obshch. Isp. Prir., Otd. Biol.,
n.s. 47: 13–19.
Henssen, A. 1963. Eine Revision der Flechtenfamilien
Lichinaceae und Ephebaceae. Symb. Bot. Upsal.
18: 1–120.
Henssen, A. and H. M. Jahns. 1973 (1974). Lichenes:
Eine Einführung in die Flechtenkunde. Stuttgart:
Thieme.
Hertig, M., W. H. Taliaferro and B. Schwartz. 1937.
The terms symbiosis, symbiont and symbiote.
J. Parasitol. 23: 326–329.
Hodkinson, B. P., F. M. Lutzoni, T. M. Loveless and
P. E. Bishop. 2006. Non-photosynthetic bacteria
and the lichen symbiosis. In: M. Bright, M. Horn,
D. Zook, S. Lücker and I. Kolar, eds. 2006.
5th International Symbiosis Society Congress:
Program, Abstracts, Participants. Gdynia:
Promare. P. 95.
Hue, A.-M. 1906. Lichenes morphologice et
anatomice disposuit. Nouv. Arch. Mus. Hist. Nat.,
sér. 4. 8: 237–272.
Kalb, K. 1987. Brasilianische Flechten 1. Die Gattung
Pyxine. Stuttgart: Cramer.
Khakhina, L. N. 1992. Concepts of Symbiogenesis.
New Haven and London: Yale University Press.
Kirk, P. M., P. F. Cannon, D. W. Minter and
J. A. Stalpers. 2008. Ainsworth and Bisby’s
Dictionary of the Fungi, ed 10. Wallingford: CAB
International.
Klebs, G. 1882. Ueber Symbiose ungleichartiger
Organismen. Biol. Centralbl. 2: 289–395.
Koerber, G. W. 1855. Systema Lichenum Germaniae.
Breslau: Trewendt and Granier.
Kolumbe, E. 1927. Purpurbakterien und Flechten.
Mikrokosmos 21: 53–55.
Krabbe, G. 1882. Entwickelung, Sprossung und
Theilung einiger Flechtenapothecien. Bot. Zeitung
(Berlin) 40: 105–116.
Kützing, F. T. 1845–1871. Tabulae Phycologicae. 20
vols. Nordhausen: Förstemann.
Lamb, I. M. 1959. Lichens. Sci. Amer. 201: 144–156.
Laundon, J. R. 1995. On the classification of lichen
photomorphs. Taxon 44: 387–389.
Leighton, W. A. 1854. Monograph of the British
Graphideae. Ann. Mag. Nat. Hist., ser. 2. 13:
436–446.
Lewis, D. H. 1985. Symbiosis and mutualism: crisp
concepts and soggy semantics. In: D. H. Boucher,
ed. 1985. The Biology of Mutualism. London and
Sydney: Croom Helm. Pp. 29–39.
Lindau, G. 1899. Beiträge zur Kenntniss der Gattung
Gyrophora. In: [S. Schwendener, honoree.] 1899.
Botanische Untersuchungen, S. Schwendener zum
10. Februar 1899 dargebracht. Berlin: Borntraeger.
Pp. 19–36.
Linnaeus, C. 1753. Species Plantarum. 2 vols.
Stockholm: Salvius.
Llano, G. A. 1950. A Monograph of the Lichen Family
Umbilicariaceae in the Western Hemisphere.
Washington, D.C.: Office of Naval Research.
Lohwag, H. 1941. Anatomie der Asco- und
Basidiomyceten. In: H. Linsbauer, ed. 1921–1943.
Handbuch der Pflanzenanatomie. 10 vols. Berlin:
Borntraeger. Vol. 6, sect., 2, pt. 3. Pp. i–xi, 1–572.
Martius, [C. F. P.] von. 1826. Auszug aus einem
Berichte des Hrn. Hofraths, Ritters v. Martius,
über den dermaligen Stand unserer Kenntnisse von
den Flechten. Flora 9: 193–204, 209–219.
Martius, C. F. P. de. 1828–1834. Icones Plantarum
Cryptogamicarum. 4 pts. Munich: For the author.
Mitchell: De Bary’s legacy
Mattirolo, O. 1883. La Simbiosi nei Vegetali. Turin:
Roux and Favale.
Mereschkowsky, C. 1905. Über Natur und Ursprung
der Chromatophoren im Pflanzenreiche. Biol.
Centralbl. 25: 593–604.
Mereschkowsky, C. 1910. Theorie der zwei Plasmaarten
als Grundlage der Symbiogenesis. Biol. Centralbl.
30: 278–288, 289–303, 321–347, 353–367.
Meyer, G. F. W. 1825. Die Entwickelung,
Metamorphose und Fortpflanzung der Flechten.
Göttingen: Vandenhoeck and Ruprecht.
Micheli, P. A. 1729. Nova Plantarum Genera.
Florence: Paperini.
Millbank, J.W. and K. A. Kershaw. 1974 (1973).
Nitrogen metabolism. In: V. Ahmadjian and M.
E. Hale, eds. 1974. The Lichens. New York and
London: Academic Press. Pp. 289–307.
Minks, A. 1900. Analysis der Flechtengattung
Umbilicaria. Mém. Herb. Boissier 22: 1–77.
Moreau, F. and [V.] Moreau. 1919. Recherches sur les
lichens de la famille des Peltigéracées. Ann. Sci.
Nat., Bot., sér. 10. 1: 29–137.
Mudd, W. 1861. A Manual of British Lichens.
Darlington: For the author.
Müller, J. 1881. Lichenologische Beiträge. Flora 64:
100–112.
Nannfeldt, J. A. and G. E. Du Rietz. 1945. Vilda
Växter i Norden: Mossor, Lavar, Svampar, Alger.
Stockholm: Natur och Kultur.
Nienburg, W. 1913. Symbiose (Flechten). In: E.
Korschelt, G. Linck, F. Oltmanns, K. Schaum,
H. T. Simon, M. Verworn and E. Teichmann,
eds. 1912–1915. Handwörterbuch der
Naturwissenschaften. 10 vols. Jena: Fischer. Vol. 9.
Pp. 929–940.
Nienburg, W. 1917. Über die Beziehungen zwischen
den Algen und Hyphen im Flechtenthallus. Z. Bot.
9: 529.
Nienburg, W. 1926. Anatomie der Flechten. Berlin:
Borntraeger.
Norman, J. M. 1872. Fuligines lichenosae eller
Moriolei. Bot. Not. 1872: 9–20.
Nylander, W. 1853. Collectanea lichenologica in
Gallia Meridionali et Pyrenaeis. Nya Bot. Not.
1853: 151–165.
Nylander, W. 1858–1869. Synopsis Methodica
Lichenum. 2 vols. Paris: Martinet.
Olivier, H. 1882–1884. Flore Analytique et Dichotomique
des Lichens de l’Orne et Départements Circonvoisins.
Autheuil: For the author.
Osswald, L. 1896. Aus dem Leben Wallroth’s. Mitth.
Thüring. Bot. Vereins, ser. 2. 9: 14–27.
Perru, O. 2006. Aux origines des recherches sur la
symbiose vers 1868–1883. Rev. Hist. Sci. Applic.
59: 5–27.
21 Persoon, C. H. 1794a. Einige Bemerkungen über die
Flechten. Ann. Bot. (Usteri) 7: 1–32, 155–158.
Persoon, C. H. 1794b. Neuer Versuch einer
systematischen Eintheilung der Schwämme. Neues
Mag. Bot. 1: 63–128.
Piercey-Normore, M. and P. T. DePriest. 2001. Algal
switching among lichen symbionts. Amer. J. Bot.
88: 1490–1498.
Poelt, J. 1965. Über einige Artengruppen der
Flechtengattungen Caloplaca und Fulgensia. Mitt.
Bot. Staatssamml. München 5: 571–607.
Poelt, J. 1969. Bestimmungsschlüssel europäischer
Flechten. Lehre: Cramer.
Poelt, J. 1974 (1973). Systematic evaluation of
morphological characters. In: V. Ahmadjian and
M. E. Hale, eds. 1974. The Lichens. New York and
London: Academic Press. Pp. 91–115.
Poelt, J. 1980. Physcia opuntiella spec. nov. und die
Lebensform der Sprossenden Flechten. Flora 169:
22–31.
Poelt, J. 1986. Morphologie der Flechten: Fortschritte
und Probleme. Ber. Deutsch. Bot. Ges. 99: 3–29.
Poelt, J. 1989. Die Entstehung einer Strauchflechte aus
einem Formenkreis krustiger Verwandter. Flora
183: 65–72.
Poelt, J. and H. Mayrhofer. 1988. Über Cyanotrophie
bei Flechten. Pl. Syst. Evol. 158: 265–281.
Quispel, A. 1943–1945. The mutual relations between
algae and fungi in lichens. Recueil Trav. Bot.
Néerl. 40: 413–541.
Quispel, A. 1951. Some theoretical aspects of
symbiosis. Antonie van Leeuwenhoek J. Microbiol.
Serol. 17: 69–80.
Rambold, G. and D. Triebel. 1992. The Interlecanoralean Associations. Berlin and Stuttgart:
Cramer.
Reinke, J. 1872. Ueber die anatomischen Verhältnissse
einiger Arten von Gunnera L. Nachr. Königl. Ges.
Wiss. Georg-Augustus-Univ. 1872: 100–108.
Reinke, J. 1894. Abhandlungen über Flechten. II. Die
Stellung der Flechten im Pflanzensystem. Jahrb.
Wiss. Bot. 26: 524–542.
Reinke, J. 1895. Abhandlungen über Flechten. IV.
Skizzen zu einer vergleichenden Morphologie des
Flechtenthallus. Jahrb. Wiss. Bot. 28: 359–486.
Richardson, D. H. S. 1999. War in the world of lichens:
Parasitism and symbiosis as exemplified by lichens
and lichenicolous fungi. Mycol. Res. 103: 641–650.
Saffo, M. B. 1993. Coming to terms with a field: Words
and concepts in symbiosis. Symbiosis 14: 17–31.
Santesson, R. 1968. Lavar: Some aspects on lichen
taxonomy. Svensk Naturvetensk. 1968: 176–184.
Sapp, J. 1994. Evolution by Association: A History of
Symbiosis. New York: Oxford University Press.
22
Huntia
15(1) 2014
Schaede, R. 1943. Die pflanzlichen Symbiose. Jena:
Fischer.
Schneider, A. 1895. Some special phylogenetic
adaptations in lichens. — 1. Bull. Torrey Bot. Club
22: 494–500.
Schwendener, S. 1869. Die Algentypen der
Flechtengonidien. Basel: Schultze.
Schwendener, S. 1872. Erörterungen zur Gonidienfrage.
Flora 55: 161–176, 177–183, 193–202, 225–234.
Scott, G. D. 1957. Lichen terminology. Nature 179:
486–487.
Sérusiaux, E. 1985. Goniocysts, goniocystangia
and Opegrapha lambinonii and related species.
Lichenologist 17: 1–25.
Sérusiaux, E., E. Fischer and D. Killmann. 2006.
Nyungwea, a new genus of lichen with goniocystproducing stipes from Rwanda and Uganda (East
Africa). Lichenologist 38: 115–121.
Smith, A. L. 1921. Lichens. Cambridge: Cambridge
University Press.
Snell, W. H. and E. A. Dick. 1957. A Glossary of
Mycology. Cambridge, Mass.: Harvard University
Press.
Sprague, T. A. 1933. Botanical terms in Pliny’s Natural
History. Bull. Misc. Inform. Kew 1: 30–40.
Stocker, O. 1975. Prinzipien der Flechtensymbiose.
Flora 164: 359–376.
Strasburger, E. 1891. Die Wechselbeziehungen der
Organismen. Deutsche Rundschau 47: 192–207.
Swinscow, T. D. V. and H. Krog. 1978. The genus
Dirinaria in East Africa. Norweg. J. Bot. 25: 157–168.
Theophrastus. 1976. De Causis Plantarum, vol. 1, bks.
1 and 2, ed. and transl. B. Einarson and G. K. K.
Link. London: Heinemann; Cambridge, Mass.:
Harvard University Press.
Theophrastus. 2003. Théophraste: Recherches sur les
Plantes [Historia Plantarum], vol. 1, bks. 1 and 2,
ed. and transl. S. Amigues. Paris: Les Belles Lettres.
Thomas, E. A. 1939. Über die Biologie von
Flechtenbildnern. Beitr. Kryptogamenfl. Schweiz
9: 4–208.
Tobler, F. 1910. Über den Begriff Symbiose in der
heutigen Biologie. Aus der Natur (Stuttgart) 6:
405–411.
Tobler, F. 1925. Biologie der Flechten. Berlin: Borntraeger.
Tobler, F. 1934. Die Flechten. Jena: Fischer.
Tønsberg, T. 1992. The sorediate and isidiate,
corticolous, crustose lichens in Norway.
Sommerfeltia 14: 1–331.
Tournefort, J. P. de. 1700. Institutiones Rei Herbariae,
ed. 2. 3 vols. Paris: Royal Press.
Tubeuf, K. von. 1895. Pflanzenkrankheiten durch
kryptogame Parasiten Verursacht. Berlin: Springer.
Tubeuf, K. von. 1897. Diseases of Plants Induced
by Cryptogamic Parasites, transl. W. G. Smith.
London: Longmans, Green.
Tuckerman, E. 1872. Genera Lichenum: An
Arrangement of North American Lichenes.
Amherst: Nelson.
Tulasne, L.-R. 1852. Mémoire pour servir à l’histoire
organographique et physiologique des lichens.
Ann. Sci. Nat., Bot., sér. 3. 17: 5–128, 153–225.
Unger, F. 1833. Algologische Beobachtungen. Nova
Acta Phys.-Med. Acad. Caes. Leop.-Carol. Nat.
Cur. 16: 523–542.
Uphof, J. C. T. 1925. The occurrence of purple bacteria
as symbionts of a lichen. Amer. J. Bot. 12: 97–103.
Vainio (Wainio), E. A. 1887. Monographia
Cladoniarum universalis. Pars prima. Acta Soc.
Fauna Fl. Fenn. 4: 1–510.
Vainio (Wainio), E. A. 1890. Étude sur la classification
naturelle et la morphologie des lichens du Brésil.
Acta Soc. Fauna Fl. Fenn. 7: 1–256.
Van Beneden, P.-J. 1873. Un mot sur la vie sociale
des animaux inférieurs. Bull. Acad. Roy. Sci.
Belgique, sér. 2. 36: 779–796.
Ventenat, E. P. 1799 (An VII). Tableau du Regne
Végétale, selon la Méthode de Jussieu. 4 vols. Paris:
Drisonnier.
Vě zda, A. 1973. Foliicole Flechten aus der Republik
Guinea (W. Afrika). I. Č as. Slez. Mus., Ser. A,
Hist. Nat. 22: 67–90.
Vě zda, A. 1979. Flechtensystematische Studien
XI. Beiträge zur Kenntniss der Familie
Asterothyriaceae (Discolichenes). Folia Geobot.
Phytotax. 14: 43–94.
Wagenitz, G. 2008. Wörterbuch der Botanik, ed. 2.
Hamburg: Nikol.
Wallert, K. 1931. Beiträge zur Symbiose von Hyphen
und Gonidien im Lichenenthallus. Bot. Arch. 33:
310–357.
Wallroth, F. W. 1825–1827. Naturgeschichte de
Flechten. 2 vols. Frankfurt: Wilmans.
Werner, R.-G. 1928. Etude biologique et
physiologique du Celidium stictarum (De Not.) Tul.
Bull. Trimestriel Soc. Mycol. France 44: 194–204.
Zopf, W. 1897. Ueber Nebensymbiose (Parasymbiose).
Ber. Deutsch. Bot. Ges. 15: 90–92.
Zukal, H. 1895. Morphologische und biologische
Untersuchungen über die Flechten (II. Abhandlung).
Sitzungsber. Kaiserl. Akad. Wiss., Wien, Math.Naturwiss. Cl., Abt. 1. 104: 1303–1395.

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